Metabolic Syndrome and Kidney Stone Disease: A Systematic Review of Literature

Abstract

Introduction:

Worldwide obesity has more than doubled since 1980 with more than 600 million obese patients in 2014. Metabolic syndrome (MetS) is the co-occurrence of metabolic abnormalities, including centrally distributed obesity, hypertension, dyslipidemia, and hyperglycemia. With a concurrent rise in the incidence of kidney stone disease, we wanted to conduct a systematic review focused on the association of MetS to nephrolithiasis.

Materials and Methods:

A systematic review was performed according to the Cochrane and preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines on all English language articles for the following relevant keywords: association, metabolic syndrome, metabolic syndrome traits, syndrome X, nephrolithiasis, kidney stones, and renal calculi. Our inclusion criteria were studies comparing the prevalence of kidney stone disease in patients with and without MetS.

Results:

The initial literature search identified 355 potentially relevant studies. After screening, 22 full text articles were reviewed and 6 (219,255 patients) were included in the final review. All studies displayed increasing odds of nephrolithiasis with increasing number of MetS traits, where patients with three or more MetS traits tended to have a higher prevalence of nephrolithiasis. Studies also showed different significant components of MetS contributing to nephrolithiasis.

Conclusions:

Our review shows a definite association of MetS with kidney stone disease. Although multifactorial in etiology, lifestyle and dietary factors seem to be increasingly important in prevention of stone disease.

Introduction

Metabolic syndrome (MetS) is the co-occurrence of metabolic abnormalities, including centrally distributed obesity, hypertension, dyslipidemia, and hyperglycemia.¹ MetS has become one of the major health challenges worldwide as it is associated with increased risk of cardiovascular diseases and type II diabetes mellitus.² Furthermore, MetS is linked with urologic diseases such as erectile dysfunction, benign prostate hyperplasia, chronic kidney disease, and kidney stones (nephrolithiasis).³ Insulin resistance is now recognized to be most commonly associated with the development of each of the components of MetS.⁴

The incidence of kidney stone disease is rising globally, and some investigators have proposed a causal link between MetS and kidney stones.⁵ Kidney stone disease is a growing problem worldwide, and in the United Kingdom, ∼720,000 individuals currently have a history of kidney stones.⁶ The aim of this study was to conduct a systematic review of the association of MetS with nephrolithiasis and consider the types of kidney stones most commonly associated with MetS.

Materials and Methods

Search strategy and study selection

The systematic review was performed according to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines.⁷ The search strategy was aimed at major electronic medical databases in the English language, among which were MEDLINE, EMBASE, PUBMED, and Web of Science Core, using the following keywords: “association,” “metabolic syndrome,” “metabolic syndrome traits,” “syndrome X,” “nephrolithiasis,” “kidney stones,” and “renal calculi.” Two reviewers (Y.W. and B.K.S.) independently screened all the titles and abstracts in an effort to minimize selection bias. The relevance of each study was assessed according to the inclusion criteria stated in Table 1; studies that did not meet the criteria were excluded.

Table 1.

Article Inclusion Criteria

Study design	Any observational (cross sectional, case–control, cohort)
Exposure	Patients with metabolic syndrome
Intervention	None
Comparator	Patients without metabolic syndrome
Outcomes	Patients with kidney stone disease

The initial literature search identified 355 potentially relevant studies (A). Their titles and abstracts were screened for relevance to the review (B, C, D), resulting in 18 potential articles (E) being retained after excluding duplicate results. The full text of these potential articles was obtained, and after applying the inclusion criteria, 12 articles were excluded (F), leaving 6 articles (G) that were included for the systematic review.

Data extraction and analysis

Two independent reviewers extracted data associating MetS to kidney stone disease from the relevant studies, as previously identified. The particular parameters extracted from the studies included were as follows: the year of study, the setting, the number of participants in the study (including the total number of affected patients), the number of male and female participants, the mean age of participants, the frequency of exposure to MetS (and its definition) predictors, the number of patients with kidney stones (and how defined), and the measure of association between MetS and kidney stone disease (the odds ratio and corresponding confidence intervals, adjusted to age and sex).

Results

The initial literature search identified 355 potentially relevant studies (Fig. 1). After screening, 22 full text articles were reviewed and 6 (219,255 patients) were included in the final review. All studies displayed increasing odds of nephrolithiasis with increasing number of MetS traits, where patients with three or more MetS traits tended to have a higher prevalence of nephrolithiasis (Tables 2 –5). There was also a different significant component of MetS contributing to nephrolithiasis. Out of the six studies, four were conducted in Korea, one in the United States, and one in Japan, but all were published between 2008 and 2013. All studies were cross-sectional analyses, except for one cohort study (Table 2), all mainly based on data obtained from hospitals or medical centers through the health screening test, national surveys, or surgical records.

FIG. 1.

Identification process for systemic review (Based on preferred reporting items for systematic reviews and meta-analyses [PRISMA] guidelines).

Table 2.

Relevant Studies Included in Review

				Number of participants				Outcome
Study	Year	Study type	Setting	Total	M:F	Mean age (years)	Predictor	Metabolic syndrome	Kidney stones
West et al.⁸	2008	Cross sectional	US	14870	7078:7792	58.0 ± 17.1	AHA, NHLBI	4949 (33.3%)	699 (4.7%)
Jeong et al.⁹	2011	Cross sectional	Korea	34895	20790:14105	50.0 ± 10.4	NCEP ATP III, AHA, NHLBI	4779 (13.7%)	839 (2.4%)
Jung et al.¹⁰	2011	Cohort	Korea	40687	22540:18147	44.9 ± 11.5	NCEP ATP III	7803 (19.2%)	609 (1.5%)
Kim et al.¹¹	2012	Cross sectional	Korea	116536	67262:49274	42.3 ± 8.4	NCEP ATP III	7107 (6.1%)	13416 (11.5%)
Cho et al.¹²	2013	Cross sectional	Korea	712	432:280	55.9	IDF	347 (48.7%)	N/M
Kohjimoto et al.³⁶	2013	Cross sectional	Japan	11555	8534:3021	52.5 ± 14.4	Number of metabolic traits	N/M	6603 (57.1%)

AHA = American Heart Association; NHLBI = National Heart, Lung, and Blood Institute; NCEP ATP III = National Cholesterol Education Program—Third Adult Treatment Panel; IDF = International Diabetes Foundation.

Table 3.

Definition of Metabolic Syndrome

MetS component	Gender	IDF (2006)	AHA (2004)	NCEP ATPIII (2001)	WHO (1999)	EGIR (1999)
Central obesity	Males	BMI >30 kg/m² and WC as per Table 2	WC >102 cm	WC >102 cm	WHR >0.9 or BMI >30 kg/m²	WC >94 cm
	Females	BMI >30 kg/m² and WC as per Table 2	WC >88 cm	WC >88 cm	WHR >0.85 or BMI >30 kg/m²	WC >80 cm
Raised triglycerides (TG)	Both	>150 mg/dL(1.7 mmol/L)	>150 mg/dL(1.7 mmol/L)	>150 mg/dL (1.7 mmol/L)	>1.695 mmol/L	>2.0 mmol/L
Reduced HDL cholesterol (HDL-C)	Males	<40 mg/dL(1.03 mmol/L)	<40 mg/dL(1.03 mmol/L)	<40 mg/dL	<0.9 mmol/L	<1.0 mmol/L
	Females	<50 mg/dL(1.29 mmol/L)	<50 mg/dL(1.29 mmol/L)	<50 mg/dL	<1.0 mmol/L	<1.0 mmol/L
Raised blood pressure (BP)	Both	Sys. >130 mm Hg or Dia. >85 mm Hg or in treatment for HT	>130/85 mm Hg or in treatment for HT	>130/85 mm Hg or in treatment for HT	>140/90 mm Hg	>140/90 mm Hg or in treatment for HT
Raised fasting plasma glucose (FPG)	Both	>100 mg/dL(5.6 mmol/L)	>100 mg/dL(5.6 mmol/L)	>110 mg/dL (6.1 mmol/L)	—	>6.1 mmol/dL
Other	Both	—	—	—	Microalbuminuria (UAER >20 μg/min or ACR >30 mg/g)	—

BMI = body mass index; WC = waist circumference; WHR = waist to hip ratio; HT = hypertension; UAER = urinary albumin excretion rate; ACR = albumin to creatinine ratio; MetS = metabolic syndrome; EGIR = European Group for the Study of Insulin Resistance.

Table 4.

Odds Ratios and 95% Confidence Interval of the Presence of Nephrolithiasis According to the Number of MetS Traits

	Number of metabolic traits (out of central obesity, hypertriglyceridemia, low HDL, hyperglycemia, and hypertension)
Odds ratio of nephrolithiasis	0	1	2	3	4	5
West et al.⁸	1.00^a	1.40 (0.88–2.25)	2.09 (1.41–3.10)	2.56 (1.63–4.03)	3.85 (2.62–5.67)	3.42 (1.92–6.09)
Jeong et al.⁹	1.00^a	1.41	1.60	2.26	1.81	2.54
Jung et al.¹⁰	1.00^a	1.49 (0.93–1.17)	1.42 (0.86–1. 10)	1.86 (1.09–1.42)	2.15 (1.07–1.52)	4.32 (1.28–2.35)
Kim et al.¹¹
Male	1.00^a	1.24 (1.15–1.34)	1.33 (1.23–1.45)		1.54 (1.41–1.68)
Female	1.00^a	1.23 (1.11–1.36)	1.40 (1.22–1.60)		1.71 (1.47–1.99)
Cho et al.¹²	1.00^a	N/M	N/M	N/M	N/M	N/M
Kohjimoto et al.³⁶	1.00^a	1.10 (1.01–1.21)	1.23 (1.09–1.39)	1.47 (1.22–1.77)	1.78 (1.22–2.66)	N/M

reference value.

HDL = high-density lipoprotein.

Table 5.

Odds Ratios (95% Confidence Interval) of the Presence of Kidney Stone Disease, Given the Presence of MetS and Each Component of MetS for the Included Studies

Metabolic syndrome trait
	Odds ratio and 95% confidence interval
				Kim
Author (number of patients)	West (14870)	Jeong (34895)	Jung (40687)	Male (67262)	Female (49274)	Cho (712)	Kohjimoto (11555)
MetS	N/M	1.71 (1.45–2.03)	1.36 (1.13–1.64)	1.33 (1.24–1.44)	1.56 (1.35–1.81)	1.93 (1.27–2.93)	N/M
Waist circumference (≥90 cm for men ≥85 cm for women)	N/M	2.44 (1.93–3.09)	1.59 (1.12–1.34)	1.14 (1.07–1.22)	1.16 (1.03–1.30)	1.24 (0.78–1.96)	1.04 (0.96–1.13)
High TG (≥150 mg/dL)	N/M	1.51 (1.22–1.88)	1.07 (0.74–0.89)	1.09 (1.03–1.16)	1.24 (1.08–1.42)	2.59 (1.71–3.91)	1.36 (1.22–1.52)
Low HDL (≤40 mg/dL for men ≤50 mg/dL for women)	N/M	0.65 (0.53–0.81)	1.12 (0.76–0.93)	1.05 (0.97–1.15)	1.18 (1.06–1.30)	0.62 (0.41–0.93)	N/M
High blood pressure (≥130/85 mm Hg)	N/M	2.18 (1.73–2.74)	1.50 (1.06–1.26)	1.19 (1.11–1.27)	1.80 (1.60–2.03)	1.34 (0.89–2.02)	1.14 (1.03–1.26)
High fasting glucose (≥100 mg/dL)	N/M	1.57 (1.26–1.95)	1.63 (1.03–1.30)	1.18 (1.10–1.26)	1.26 (1.12–1.42)	1.91 (1.25–2.92)	1.00 (0.87–1.15)

Most of these studies used the National Cholesterol Education Program—Third Adult Treatment Panel's (NCEP ATP III) definition of MetS, which is similar to the International Diabetes Federation (IDF) definition of MetS, although with minor variations in threshold measurements.¹³ Table 4 shows a dose–response relationship between number of MetS traits and stone frequency in all six studies along with relevant data. MetS frequency and the prevalence of stones varied considerably. All six studies showed a different significant trait of MetS contributing to nephrolithiasis (Table 5). Kim et al. reported high blood pressure as having a significant association with MetS,¹¹ while Cho et al. identified high triglyceride as the most significant trait of MetS associating with nephrolithiasis.¹²

Overall, the methodologic quality of the included studies was poor. There have been a limited number of studies on the association of MetS with kidney stone disease worldwide, and the included studies are predominantly carried out in the Far East. Out of these, the majority of the studies are cross sectional, the weakest design for assessing the causal link between two conditions. A quality assessment of the included studies was performed using the strengthening the reporting of observational studies in epidemiology (STROBE) guidelines (Table 6), along with a matrix of the author's judgment of risk of bias items for the considered studies (Table 7).

Table 6.

Quality Assessment of the Included Studies Using the STROBE Guidelines

	Kohjimoto	Cho	Kim	Jung	Jeong	West
Introduction
Objectives, scientific background, and the rationale for investigation being reported.	Y	Y	Y	Y	Y	Y
Methods
Study design, setting, locations, and relevant dates.	Y	Y	Y	Y	Y	Y
Eligibility criteria and the sources and methods of selections of patients.	Y	Y	Y	Y	Y	Y
All outcomes, predictor, exposures, and diagnostic criteria.	N	N	Y	Y	Y	Y
Sources of data and details of methods of assessment (measurement).	Y	Y	Y	Y	Y	Y
Potential sources of bias.	N	N	N	N	N	Y
How quantitative variables were handled and which groupings were chosen and why.	Y	Y	Y	Y	Y	Y
How missing data were addressed.	Y	N	N	N	N	N
Analytic methods described.	Y	Y	Y	Y	Y	Y
Results
Numbers of participants at each stage of study reported.	Y	Y	Y	Y	Y	Y
Numbers of outcomes event or summary measures over time reported.	Y	Y	Y	Y	Y	Y
Unadjusted estimates, cofounder-adjusted estimates, and their confidence interval.	N	Y	Y	Y	Y	Y
Limitations of the study.	Y	Y	Y	Y	Y	Y

STROBE = strengthening the reporting of observational studies in epidemiology.

Table 7.

Risk Bias Assessment

	West	Jeong	Jung	Kim	Cho	Kohjimoto
Sequence generation	−	−	−	−	+	+
Allocation concealment	−	+	+	+	+	+
Blinding of participants and personnel	−	+	+	+	+	+
Incomplete outcome data	−	−	?	−	−	+
Selective outcome reporting	−	+	+	+	+	+
Other sources of bias	?	+	−	−	−	−

+ = high risk; − = low risk; ? = unclear.

There are several strengths and limitations of this systematic review. The main strengths are that the review is based on the standard recommended search of literature in addition to having been reviewed by two independents reviewers. The appropriateness of inclusion criteria is demonstrated in that it resulted in a number of studies addressing the review question, with participants being similar across studies. However, the literature contains variation in definitions of MetS. Similarly, there are variations in assessment methods for kidney stones, as some studies were based on retrospective search of patients who underwent surgical intervention in clinical settings, whereas others were based on questionnaires on patients' medical history of kidney stone disease or self-reported history of kidney stone disease. The results were reported in odds ratio and their corresponding confidence intervals for the odds of kidney stones, given MetS status. After being adjusted for age, gender, and other covariates, the presence of Mets was found to significantly increase the odds of kidney stone disease.

Discussion

Definitions of MetS

Different definitions of MetS have been proposed, reviewed, recommended, and even questioned over the decades.¹⁴ The American Heart Association (AHA),¹⁵ the World Health Organization (WHO),¹⁶ the European Group for the Study of Insulin Resistance (EGIR),¹⁶ and the NCEP ATP III¹⁷ have each published their own definitions. While slightly differing in the details, all of them seem to agree on certain core components of MetS. These core components include central obesity, dyslipidemia, hypertension, and insulin resistance.

The WHO diagnostic criteria of MetS require the presence of diabetes mellitus, impaired glucose tolerance, impaired fasting glucose, or insulin resistance along with any two (or more) of the core components. Similarly, the EGIR classification requires a patient to exhibit insulin resistance along with two of the other core components to classify for MetS. However, studies suggest that the IDF definition of MetS tends to be reliable and indeed appropriate for certain ethnic groups, taking particular note of MetS prevalence.¹⁸ The IDF consensus worldwide definition of MetS is a universally accepted diagnostic tool for MetS.^1,19,20

Obesity and kidney stone diseases

Obesity, especially central obesity, is associated with the occurrence and recurrence of kidney stones due to metabolic alterations.^21,22 Lee et al. reported increased excretion of urinary uric acid, sodium, calcium, and citrate in obese stone formers, along with an increased incidence of symptomatic uric acid stones.²³ Other studies also confirm that kidney stones in obese patients are generally composed mainly of calcium oxalate and uric acid.²⁴ The issues of obesity and kidney stone disease have recently started drawing attention, as the National Health and Nutrition Examination Survey (NHANES) predicted that by 2030, the impact of obesity on kidney stone formation prevalence will have increased by 0.36%, with annual treatment costs projected to rise by ∼157 million US dollars as a result of this alone. Coupling this with population growth and other factors, the estimated treatment cost would then increase past 1 billion US dollars by 2030.²⁵

The urinary pH strongly influences the composition of stone formation; an acid urine pH promotes the formation of uric acid stone, whereas an alkaline urine pH promotes the formation of calcium phosphate-containing stones.²⁶ The pathophysiology of uric acid stone formation caused by MetS is a consequence of inappropriate acid urine, which is secondary to insulin resistance.²⁷ Strohmaier et al. revealed that insulin resistance is the most important factor of MetS and kidney stone formation, since insulin resistance decreases the production and transport of ammonia, resulting in a low urine pH.²⁸ Therefore, uric acid stone formation is a renal manifestation of MetS.²⁹ In contrast, calcium oxalate stones, which are the most common composition of kidney stones in patients with MetS, are reported to be affected little by any MetS trait.³⁰ Sakhaee's studies demonstrated that the MetS influences the excretion of calcium and supersaturation of calcium oxalate but, when adjusted for variables known to affect urinary calcium, does not impose a great effect on calcium oxalate stone formation³¹ compared with other studies linking uric acid kidney stone disease with MetS.³² Insulin resistance has also been shown not to influence calcium excretion in patients with idiopathic hypercalciuria.³³ However, highly acid urine leading to precipitation of uric acid crystals may also enhance calcium oxalate crystallization and calcium oxalate stone disease by the process of heterogeneous nucleation.³⁴

Thus, it could be reasoned that insulin resistance might be a pathogenic mechanism in MetS kidney stone disease. This statement is further supported by a study showing insulin, rather than other hormones, to be associated with kidney stone disease.³⁵

MetS components associated with kidney stone disease

Kidney stone disease is multifactorial, and multiple studies have demonstrated the association of different components of MetS to kidney stone disease.^8

–12,36 Some studies reveal that individual factors of MetS have a possible causal link with kidney stone disease: diabetes, hypertension, dyslipidemia, and obesity.^37
–39 Weinberg et al. stated that patients with high fasting plasma glucose had increased odds of having kidney stone disease, with a significant odds ratio of 2.29 (1.8–3.12).³⁸ Cupisti et al. presented a possible relationship between hypertension and kidney stone disease, which has a similar pathophysiologic mechanism as diabetes for insulin resistance.³⁷ However, only HDL in dyslipidemia was shown to have a greater association with kidney stone diseases compared with other lipid panels.³⁹ Hence, the components of MetS are equally important and may be interrelated. The relationships of these individual factors contributing to MetS would require further research and investigation into the details of the mechanism.

Management of kidney stone disease with MetS

Several guidelines are available to provide a clinical framework for diagnosis, follow-up, and prevention of kidney stone disease.⁴⁰ Metabolic screening is an important part of investigating kidney stone disease. The American Urological Association has provided guidelines on the appropriate initiation of a metabolic evaluation in selected patients and recommendations for the initiation, and follow-up, of medication and/or dietary measures in certain cases.⁴¹

Medical treatment for kidney stone disease in patients with MetS depends upon the underlying medical abnormalities detected, for example, potassium citrate for urine acidity.^42,43 Patients who are considered for bariatric surgery are at risk of both kidney stone disease and nephropathy predominantly as a consequence of enteric hyperoxaluria; preoperative counseling, monitoring of renal function, and stone screening are necessary for these patients.⁴⁴

Prevention of kidney stone disease in MetS

Lifestyle modification is the most potent method for the prevention of kidney stone formation in patients with MetS, particularly patients who are obese. Notably, the impact of weight loss is significant to the extent that it markedly improves all aspects of MetS.⁴⁵ Increasing physical activity and decreasing caloric intake by reducing portion sizes will improve MetS abnormalities, even in the absence of weight loss. Meal replacements are also equally effective as the structured weight loss diet for losing weight.⁴⁶ A diet that includes more fruits, vegetables, whole grains, monounsaturated fats, and low-fat dairy products will benefit most patients with MetS. A recent study suggested that fish consumption may likewise prevent or improve metabolic health and have a protective role in MetS.⁴⁷ The combination of diet and exercise intervention has been found to be significantly more effective than diet or exercise on their own in the prevention of kidney stones in people with MetS.⁴⁸

Conclusions

Worldwide obesity has more than doubled since 1980 with more than 600 million obese patients in 2014.⁴⁹ The association of obesity with kidney stone disease has recently started drawing attention, as NHANES predicted that by 2030, the impact of obesity on kidney stone formation prevalence will have increased by 0.36%, with annual treatment costs projected to rise by ∼157 million US dollars as a result of this alone. Coupling this with population growth and other factors, the estimated treatment cost would then increase past 1 billion US dollars by 2030.²⁵

Growing evidence shows a direct correlation between MetS and kidney stone disease.⁵⁰ The recurrence rate of kidney stone is high, with a 50% chance of forming a second stone within 7 years if causal factors and appropriate intervention are not undertaken.⁵¹ There are several pharmacotherapies that are available to prevent stone formation in patients with MetS, but lifestyle changes, in particular dietary and exercise interventions, must not be forgotten as a therapeutic intervention for the prevention of both formation and recurrence of kidney stones. Such changes may not only help in the prevention of kidney stones but also in preventing and treating obesity, hypertension, coronary artery disease, as well as the MetS itself.

Author Disclosure Statement

No competing financial interests exist.

Footnotes

Abbreviations Used

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